Genome-wide screens of genetic variation can reveal signatures of population-specific selection implicated in adaptation and speciation. Yet, unrelated processes such as linked selection arising as a consequence of genome architecture can generate comparable signatures across taxa. To investigate prevalence and phylogenetic stability of linked selection, we took a comparative approach utilizing population-level data from 444 re-sequenced genomes of three avian clades spanning 50 million years of evolution. Levels of nucleotide diversity (π),population-scaled recombination rate (ρ), genetic differentiation (FST, PBS) and sequence divergence (Dxy) were remarkably similar in syntenic genomic regions across clades. Elevated local genetic differentiation was associated with inferred centromere and sub-telomeric regions. Our results support a role of linked selection shaping genome-wide heterogeneity in genetic diversity within and between clades. The long-term conservation of diversity landscapes and stable association with genomic features make the outcome of this evolutionary process in part predictable.